Abstract
The anatomy and innervation of the lateral external muscle and sensory cells located in the ventral region of pregenital abdominal segments were examined at the larval and adult stages ofTenebrio molitor (Coleoptera). All seven muscles located in this region degenerate during the pupal stage, whilst only the lateral external median (lem) appears in the adult. Backfillings of the motor nerve innervating this muscle reveal that, at both larval and adult stages, it is innervated by ten neurons. Intracellular records from the muscle fibres show that two neurons are inhibitory, and at least five are excitatory. There are also two unpaired neurons. A variety of sensory organs are located in the ventral region of the larvae, whilst only campaniform sensilla are found in the adult. At both stages, the innervation pattern of the sensory nerve branches is very similar. Also, the central projections of the sensory cells occupy similar neuropilar areas. Finally, prolonged intracellular records from the lem muscle revealed that, at the larval stage, it participates only in segmental or intersegmental reflexes, whilst in the adult it has a primary expiratory role in ventilation. The results show that extensive changes occur in the number of muscles located in the ventral region of the pregenital abdominal segments, as well as in the arrangement and number of sensory neurons, in the structure of the exoskeleton, and even in the central nervous system. In contrast, only minor changes are observed in the sensory and motor nerve branches, in the sensory projections, and in the number and the location of the motoneurons innervating the lateral external median muscle.
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Bacon JP, Altman JS (1977) A silver intensification method for cobalt-filled neurones in wholemount preparations. Brain Res 138:359–363
Bässler U (1986) On the definition of central pattern generator and its sensory control. Biocybernetics 54:65–69
Booker R, Truman JW (1987) Postembryonic neurogenesis in the CNS of the tobacco hornworm,Manduca sexta: I. Neuroblast arrays and the fate of their progeny during metamorphosis. J Comp Neurol 255:548–559
Breidbach O (1987) The fate of persisting thoracic neurons during metamorphosis of the meal beetleTenebrio molitor (Insecta: Coleoptera). Roux's Arch Dev Biol 196:93–100
Breidbach O (1988) Reorganization of identified neurons during the metamorphosis of the meal beetle — aspects for an analysis of neuronal regeneration. Monogr Dev Biol 21:105–111
Breidbach O (1989) Fate of descending interneurons in the metamorphosing brain of an insect, the beetleTenebrio molitor L. J Comp Neurol 290:289–309
Breidbach O (1990a) Metamorphic changes in the central projections of hair sensilla inTenebrio molitor L (Insecta: Coleoptera). Cell Tissue Res 259:159–176
Breidbach O (1990b) Serotonic immunoreactive brain interneurons persist during metamorphosis of an insect: A development study of the brain ofTenebrio molitor L. (Coleoptera). Cell Tissue Res 259:345–360
Breidbach O (1990c) Constant topological organization of the coleopteran metamorphosing nervous system: Analysis of persistent elements in the nervous system ofTenebrio molitor. J Neurobiol (21)7:990–1001
Breidbach O, Dircksen H (1989) Proctolin — immunoreactive neurons persist during metamorphosis of an insect: A developmental study of the ventral nerve cord ofTenebrio molitor (Coleoptera). Cell Tissue Res 257:217–225
Breidbach O, Kutsch W (1990) Structural homology of identified motoneurons in larval and adult stages of hemi- and holometabolus insects. J Comp Neurol 297:392–409
Burrows M (1973) Physiological and morphological properties of the metathoracic common inhibitory neuron of the locust. J Comp Physiol 82:59–78
Campbell IJ (1961) The anatomy of the nervous system of the mesothorax ofLocusta migratoria migratorioides R and F. Proc Zool Soc (London) 137:403–432
Casaday GB, Camhi JM (1976) Metamorphosis of flight motor neurons in the mothManduca sexta. J Comp Physiol 112:143–158
Chapman RF (1975) Mechanoreception. In: Bullough WS (ed) The insects: structure and function. English Universities Press, London, p 597
Crossley AC (1978) The morphology and development of theDrosophila musculature system. In: Ashburner A, Wright TRF (eds) Genetics and biology of Drosophila. Academic Press, London New York San Francisco, pp 499–560
Edwards JS (1969) Postembryonic development and regeneration of the insect nervous system. Adv Insect Physiol 6:97–137
Evans PD, O'Shea (1977) The identification of an octopaminergic neuron and the modulation of a myogenic rhythm in the locust. J Exp Biol 73:235–260
Hoyle G, Dagan D, Moberly B, Colquhoun W (1974) Dorsal unpaired median insect neurons make neuro-secretory endings on skeletal muscles. J Exp Zool 187:159–165
Giebultowicz JM, Truman JW (1984) Sexual differentiation in the terminal ganglion of the mothManduca sexta: role of sex-specific neuronal death. J Comp Neurol 226:87–95
Kalogianni E, Consoulas C, Theophilidis G (1989) Anatomy and innervation of the abdominal segmental muscles in larval and adultTenebrio molitor (Coleoptera). J Morphol 202:271–279
Karnovsky JM (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy (abstract). J Cell Biol 27:137
Kent KS, Levine RB (1988a) Neural control of leg movements in a metamorphic insect: Sensory and motor elements of the larval thoracic legs inManduca sexta. J Comp Neurol 271:559–576
Kent KS, Levine RB (1988b) Neural control of leg movements in a metamorphic insect: Persistence of larval leg motor neurons to innervate the adult legs ofManduca sexta. J Comp Neurol 276:30–43
Klaasen LW (1982) Effect of octopamine and other biogenic amines on developing neuromuscular junctions ofManduca sexta (abstract). Neuroscience 6:627
Klaasen LW, Kammer AE (1980) Modulation of neuromuscular transmission by octopamine in developing adult moths (abstract). Neuroscience 6:627
Lakes-Harlan R, Pollack GS, Merritt DJ (1991) From embryo to adult: Anatomy and development of a leg sensory organ inPhormia regina, Meigen (Insecta: Diptera): II. Development and persistence of sensory neurons. J Comp Neurol 308:200–208
Lee WJ (1964) A study of the development of the musculature from the larva to adult inTenebrio molitor L. (Tenebrionidae, Coleoptera). Ph. D Thesis, University of Minnesota
Levine RB (1984) Changes in neuronal circuits during insect metamorphosis. J Exp Biol 112:27–44
Levine RB, Truman JW (1982) Metamorphosis of the insect nervous system. Changes in morphology and synaptic interactions of identified neurons. Nature 299:250–252
Levine RB, Truman JW (1985) Dentritic reorganisation of abdominal motoneurons during metamorphosis of the mothManduca sexta. J Neurosci (5) 9:2424–2431
Miller A (1965) Internal anatomy of the imago ofDrosophila melanogaster In: Demerec M (ed) Biology of Drosophila. Haffner Publishing Company, New York London, pp 420–535
Ogonowski MM, Lang F (1979) Histochemical evidence for enzyme differences in crustacean fast and slow muscle. J Exp Zool 207:143–151
Pearson KG, Fourtner CR (1973) Identification of the somata of common inhibitory motoneurons in the metathoracic ganglion of the cockroach. Can J Zool 51:859–866
Silverman H, Charlton MP (1980) A fast-oxidative crustacean muscle: histochemical comparison with other crustacean muscle. J Exp Biol 211:267–277
Taylor HM, Truman JW (1974) Metamorphosis of the abdominal ganglia of the tobacco hornwormManduca sexta: Changes in populations of identified motoneurons. J Comp Physiol 90:367–388
Thorn RS, Truman JW (1989) Sex-specific neuronal respecification during the metamorphosis of the genital segments of the tobacco hornworm mothManduca sexta. J Comp Neurol 284:489–503
Truman JW (1983) Programmed cell death in the nervous system of an adult insect. J Comp Neurol 216:445–452
Truman JW, Levine RB (1983) Cellular events in the nervous system during metamorphosis in the insect,Manduca sexta. In: Barker J, McKelvy J (eds) Current methods in cellular neurobiology. Wiley, New York, pp 16–17
Truman JW, Reiss SE (1976) Dentritic reorganization of an identified motoneuron during metamorphosis of the tobacco hornworm moth. Science 192:477–479
Truman JW, Schwartz LM (1984) Steroid regulation of neural death in the moth nervous system. J Neurosci 4:274–280
Tsujimura H (1988) Metamorphosis of wing motor system in the silk moth,Bombyx mori L. (Lepidoptera: Bombycidae): Anatomy of the sensory and motor neurons that innervate larval mesothoracic dorsal musculature, stretch receptors, and epidermis. Int J Insect Morphol Embryol 17:367–380
Tsujimura H (1989) Metamorphosis of wing motor system in the silk moth,Bombyx mori: origin of wing motor neurons. Dev Growth Differ 31:331–339
Weeks JC, Truman JW (1985) Cellular interactions between a muscle and its motoneuron are not involved in their endocrin-mediated deaths during metamorphosis in the tobacco hornwormManduca sexta. Neurosci Abstr 9:605
Williams GIA, Caveney S (1980) Changing muscle patterns in a segmental epidermal field. J Embryol Exp Morphol 58:13–33
Wright BR (1976) Limb and wing receptors in insects chelicerates and myriapods. In: Mill PJ (ed) Structure and function of proprioceptors in the invertebrates. Chapman and Hall, London, pp 323–386
Yang ZQ, Burrows M (1983) The identification of motor neurones innervating an abdominal ventilatory muscle in the locust. J Exp Biol 107:115–127
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Correspondence to: G. Theophilidis
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Paspalas, C., Consoulas, C. & Theophilidis, G. The fate of specific motoneurons and sensory neurons of the pregenital abdominal segments inTenebrio molitor (Insecta : Coleoptera) during metamorphosis. Roux's Arch Dev Biol 202, 204–213 (1993). https://doi.org/10.1007/BF02427881
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DOI: https://doi.org/10.1007/BF02427881